This article was originally published in the Encyclopedia of Neuroscience published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non- commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who you know, and providing a copy to your institution’s administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institution’s website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial Searcy W A and Nowicki S (2009) Sexual Selection and the Evolution of Animal Signals. In: Squire LR (ed.) Encyclopedia of Neuroscience, volume 8, pp. 769- 776. Oxford: Academic Press. Author's personal copy Sexual Selection and the Evolution of Animal Signals 769 Sexual Selection and the Evolution of Animal Signals W A Searcy , University of Miami, Coral Gables, FL, such as mammals and birds, with extensive parental USA care. Largely as a result of these parental investment S Nowicki , Duke University, Durham, NC, USA patterns, females typically have lower maximal rates ã 2009 Elsevier Ltd. All rights reserved. of reproduction. Thus sexual biases in both parental investment and maximal rates of reproduction predict the predominance of female choice. Introduction Many of the greats of evolutionary biology who followed Darwin were skeptical of the importance of Darwin defined sexual selection in On the Origin of female choice as a selective mechanism. Alfred Russel Species as a mechanism that ‘‘depends, not on a strug- Wallace, for example, thought ‘‘it almost inconceiv- gle for existence, but on a struggle between the males able that female preference could have been effective for possession of the females; the result is not death in the way suggested,’’ that is, in bringing about the to the unsuccessful competitor, but few or no off- evolution of male displays. Such skepticism may be spring.’’ Thus sexual selection is a form of selection attributed in part to unwary references by Darwin to in which variation in fitness is caused by variation in an ‘‘aesthetic capacity’’ in female animals, allowing mating success, and which favors traits associated them ‘‘an appreciation of the beautiful in sound, col- ... with enhanced mating success. Darwin’s initial descrip- our or form. ’’ Attribution of an esthetic sense to tion of sexual selection – ‘‘a struggle between the males animals, or even of simple choice, implied a higher for possession of the females’’ – implies that he had in level of cognition than many scientists were willing to mind only aggressive competition among males, but accede to birds of paradise and peafowl, let alone to the paragraphs that followed make it clear that Darwin crickets and moths. Nowadays, however, evolution- recognized that the struggle ‘‘is often of a more peaceful ary biologists realize that the kinds of mating pre- character,’’ with males competing through displays to ferences observed in many animals do not actually attract females for mating. Darwin later expanded on call for much in the way of cognitive ability. The these themes in The Descent of Man, and Selection words ‘choice’ and ‘preference’ currently are used to in Relation to Sex, treating at length both of the describe biases in the probability that females will major components of sexual selection: intrasexual mate with males having certain traits, without regard selectionthrough aggressive competition and intersex- to whether these biases require cognitive processing. ual selection through mate choice. Here we concentrate From an evolutionary perspective, what matters most on the intersexual, mate choice component and its is whether female mating behavior is biased in a way effects on animal communication. that affects male mating success, not the mechanism – Darwin thought that it was almost universally true cognitive or otherwise – that underlies the bias. More- that males are more eager to mate than are females over, it is now realized that, though we may be and that as a consequence, females are the sex that tempted to label the preferences of nonhuman animals exercises mate choice. This pattern is still considered as esthetic, these preferences do not necessarily mesh the rule, though exceptions are now recognized, both with our own sense of what is beautiful, as should be cases in which males and females are almost equally conceded by anyone who observes such preferences as selective and cases in which male choice of mates that of female common grackles for the songs of their predominates. Theory successfully explains both the own species. rule and the exceptions, either on the basis of the Another reason for Wallace’s skepticism about relative parental investment made by the two sexes female choice was the lack of empirical evidence for or, almost equivalently, on the basis of maximal rates the hypothesized preferences. One could in theory of reproduction. In brief, the sex that makes the explain the evolution of the extravagant song of a greater investment in producing and rearing offspring, nightingale or the brilliant coloration of a coral reef or that has the lower maximal rate of reproduction, fish by positing the appropriate female preferences, but limits reproduction in the other sex; consequently, the there was no evidence that the required preferences limited sex competes to mate, while the limiting sex actually existed. Since Wallace’s day, however, and exercises choice. Females typically provide greater in particular during the past 30 years, a great deal of parental investment than males do, whether in taxa evidence has supported the existence of female pre- in which both sexes invest only in gametes or in groups ferences in various animal groups. More often than Encyclopedia of Neuroscience (2009), vol. 8, pp. 769-776 Author's personal copy 770 Sexual Selection and the Evolution of Animal Signals not, the female preference is for a male trait that we show a preference based on ‘asynchrony interval,’ the would label as a signal, and which is therefore an time interval between the onsets of the two pulses in a element of animal communication. pair. This preference function shows yet another shape, with females discriminating against signals with very Evidence of Female Preferences Based short asynchrony intervals but treating all signals with on Male Signals higher intervals equivalently (Figure 1(d)). Further experiments confirmed these preferences An excellent illustration of female preferences based under more naturalistic conditions. Series of females on male signal characteristics is provided by the were allowed to choose between sets of four males con- work of Michael Greenfield and colleagues on female fined in separate cages. Approach was again assumed to choice in the lesser wax moth (Achroia grisella). indicate choice. Partial regression coefficients indicate Lesser wax moths are obligate symbionts of honey- that the number of females attracted by a male is bees (Apis mellifera), feeding as larvae on honeycomb significantly positively related to each of the three and other materials found in honeybee colonies. As signal characteristics mentioned above: call ampli- adults, male lesser wax moths aggregate in the vicin- tude, call rate, and asynchrony interval. ity of a honeybee colony and produce sexual displays These results from lesser wax moths are typical of a to attract females for mating. The primary display is large body of evidence from insects and anurans an ultrasonic acoustic signal produced by fanning the showing female preferences for male displays that wings.The sound-producing organs are a pair of have greater acoustic energy. In a review of results tymbals located at the base of the forewings; these on several dozen species of frogs and insects, Gerhardt are hardened, platelike structures that produce sound and Huber found that females prefer higher male call when they buckle either in or out. A single stroke of rates over lower in the great majority of the studied the wings produces a pair of sound pulses, one from species. Similarly, females typically prefer male calls the left tymbal and one from the right, slightly offset of longer duration to shorter ones. By contrast, pre- in time ( Figure 1(a)). Pairs of pulses are produced by ferences based on the rate of pulses within a call or on both the downstroke and the upstroke of the wings. carrier frequency are most often stabilizing, with calls Males also release pheromones in conjunction with of average properties preferred over either extreme. wing fanning, but playback of the sound from a loud- Exceptions to all these generalizations have been speaker is as effective in attracting females as is a live found; in particular, females in several species of signaling male, indicating that the ultrasonic signal is frogs show preferences for male calls of lower fre- the only cue essential for mate attraction. quency than the population mean. Female lesser wax moths have been tested in the In birds, female preferences based on vocalization laboratory for preferences based on acoustic proper- rates are again observed quite commonly, with females ties of male sounds, using phonotaxis to a loud- consistently preferring males that